The Feedback-Related Negativity, but not Frontal Midline Theta, Reflects Prediction Errors During Both Positive and Negative Reinforcement

Dopamine signals convey neural representations of past rewarding and aversive experiences by encoding prediction errors that drive reinforcement learning. The feedback-related negativity (FRN) is a component of the event-related potential that is sensitive to valenced feedback; Holroyd & Coles (2002) theorize that the reinforcing properties of the FRN derive from dopaminergic prediction error signals. Reinforcement processing has also been studied using frontal midline theta (4-7 Hz) activity, which peaks around the same time as the FRN and increases in response to unexpected events compared to expected events. We recorded EEG while subjects completed a Monetary Incentive Delay task that included positive reinforcement and negative reinforcement conditions with multiple levels of reward and punishment, as well as control conditions that had no reinforcement value. We show that despite temporal overlap of FRN and frontal midline theta, these measures index dissociable neuro-cognitive mechanisms. Results suggest that the FRN, but not frontal midline theta, is specifically sensitive to reinforcing outcomes. The FRN represented prediction errors in both positive and negative reinforcement, while frontal theta instead represented unexpected outcomes regardless of reinforcement value. Furthermore, the FRN was sensitive to the point value of feedback in both positive and negative reinforcement, while theta activity was not influenced by feedback point value. These results are consistent with the theory that the FRN is influenced by dopaminergic signaling, and suggest that frontal theta instead represents local processing of unexpected events regardless of whether they are reinforcing or not.